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Bloom & Kolmann Et Al 2019 Miniaturization in New World

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Bloom & Kolmann Et Al 2019 Miniaturization in New World Received: 9 September 2019 Accepted: 14 November 2019 DOI: 10.1111/jfb.14205 REGULAR PAPER FISH Mode of miniaturisation influences body shape evolution in New World anchovies (Engraulidae) Devin D. Bloom1,2 | Matthew Kolmann3 | Kimberly Foster1 | Helen Watrous1 1Department of Biological Sciences, Western Michigan University, Kalamazoo, Abstract Michigan, USA We explored the macroevolutionary dynamics of miniaturisation in New World 2 Institute of the Environment & Sustainability, anchovies by integrating a time-calibrated phylogeny, geometric morphometrics and Western Michigan University, Kalamazoo, Michigan, USA phylogenetic comparative methods. We found that the paedomorphic species 3Department of Biological Sciences, George Amazonsprattus scintilla occupies a novel region of shape space, while the dwarf spe- Washington University, Washington, DC, USA cies Anchoviella manamensis has an overall shape consistent with other anchovies. Correspondence We found that miniaturisation did not increase overall clade disparity in size or shape Devin D. Bloom, Department of Biological Sciences, Western Michigan University, 1903 beyond the expectations of Brownian motion, nor were there differences in rates of W. Michigan Avenue, Kalamazoo, MI size or shape evolution among clades. Overall, our study shows that while the mode 49008-5410, USA. Email: [email protected] of miniaturisation influences shape evolution, the phenotypic novelty produced by the evolution of miniaturisation did not seem to alter macroevolutionary dynamics. Funding information Directorate for Biological Sciences, Grant/ KEYWORDS Award Number: DEB 1754627 body size, Engraulidae, geometric morphometrics, macroevolution, miniaturisation, Neotropics 1 | INTRODUCTION with an increase in morphological variation and phenotypic novelty in a lineage (Hanken, 1986). Unlike developmentally truncated paedo- The evolution of extreme body size offers insight into the limits of morphic taxa, dwarf species resemble larger-bodied relatives (Britz phenotypic evolution in animals. The patterns and processes associ- et al., 2009; Ruber et al., 2007). However, the contribution of dwarf ated with large body size are well studied and evidence for selection species on the phenotypic diversity of a clade is largely unknown. If favouring large body size is omnipresent at both population (Roff, dwarf species retain the same bauplan and shape dimensions as larger 1991; Stearns, 1977) and macroevolutionary scales (Albert & Johnson, relatives, we predict they will reside in the same region of morphospace as non-miniaturised relatives. Under this scenario, dwarf species may not 2012; Jaffe et al., 2011; Pimiento et al., 2019; Slater et al., 2017; Ver- be associated with an increase in morphological variation. Alternatively, meij, 2012). Miniaturisation, or the extreme decrease in body size, has dwarf species may experience shifts that result in changes to the mor- evolved repeatedly in animals (Hanken & Wake, 1993) and a high phological diversity within a clade (Alberch et al., 1979; Britz & Conway, diversity of miniaturised fishes occur in the Neotropics (Goulding 2009; Britz et al., 2009; Buckup, 1993; Turner et al., 2007; Weitzman & et al., 1988; Roberts, 1984; Steele & López-Fernández, 2014; Vari, 1988) Few studies have explored the macroevolutionary patterns Weitzman & Vari, 1988). However, the processes shaping the evolu- and processes associated with different modes of miniaturisation nor tion of miniaturisation and the resulting phenotypic patterns are have directly compared the effect of modes of miniaturisation on pheno- poorly known (Blackenhorn, 2000), limiting our understanding of the typic evolution (Blackenhorn, 2000). role of extremely small body size in diversification. Miniaturisation has evolved numerous times in fishes, particularly in The evolution of miniaturisation can have a profound effect on South American freshwater rivers (Weitzman & Vari, 1988). In this phenotypic evolution and is often linked to morphological novelty study we use New World anchovies (Engraulidae) to explore the evolu- (Britz et al., 2009; Hanken, 1986; Yeh, 2002). There are two modes of tion of miniaturisation. New World anchovies are divided into two miniaturisation: paedomorphism and dwarfism. Paedomorphic species major clades: the marine clade and the South American clade (Bloom & typically arise due to shifts in the developmental process (Alberch Lovejoy, 2012). The marine clade includes approximately 45 species et al., 1979; Lovejoy, 2000) and are hypothesised to be associated and is dominated by near-shore, schooling and largely planktivorous J Fish Biol. 2019;1–8. wileyonlinelibrary.com/journal/jfb © 2019 The Fisheries Society of the British Isles 1 2 FISH BLOOM ET AL. species found in both the eastern Pacific and western Atlantic Oceans. experiments or surgical procedures on live specimens. No part of this The speciose genus Anchoa Jordan & Evermann 1927 comprises most study involved live fishes. of the species diversity in the marine clade and along with several spe- cies of Anchoviella Fowler 1911, tend to have superficially similar exter- 2.1 | Morphometric data and analysis nal morphology and relatedly, seem to occupy similar ecological niches. This marine clade also includes several medium-sized, deep-bodied spe- We used body size data from Bloom et al. (2018). These authors com- cies in the genera Cetengraulis Günther 1868 and Anchovia Jordan & piled maximum LS body size data for all Clupeiformes from Fishbase Evermann 1895, as well as elongate species in the genus Engraulis (Froese & Pauly, 2017), Whitehead et al. (1988) and Carpenter (2002), Cuvier 1816. The South American clade, comprising six genera and which we pruned to focus on New World anchovies. Standard lengths more than 20 species, is ecologically diverse (Bloom & Egan, 2018; were log-transformed for subsequent analyses. For comparative ana- Bloom & Lovejoy, 2012; Egan et al., 2018a) and variable in size (Bloom lyses we used a published, multi-gene, time-calibrated phylogeny for et al., 2018). The majority of species in the South American clade are all Clupeiformes (Bloom & Lovejoy, 2014). The original phylogeny endemic to freshwater rivers in South America, but several species (e.g., included 52 New World anchovy species and was pruned to match Lycengraulis grossidens (Spix & Agassiz 1829) and Lycengraulis poeyi our size and shape data (described below; Figure 1). (Kner 1863)) are marine species that are derived from reversals back to Geometric morphmetrics is ideal for quantifying shape diversity of oceanic habitats and occur along the coasts of northern South America. miniaturised species because it characterises morphometric shape There are two species of miniaturised anchovies, Amazonsprattus independent of size, location and orientation (Angielczyk & Feldman, scintilla Roberts 1984 (<20 mm standard length; LS), a putatively paedo- 2013; Zelditch et al., 2004). Images of museum specimens of 45 spe- morphic species and Anchoviella manamensis Cervigón 1982 (<20 mm cies of Anchovies were taken from the left lateral side using a Nikon LS), a dwarf species (Lavoué et al., 2010; Weitzman & Vari, 1988; D750 and a 60 mm macro lens (www.nikon.com). Bent, warped, or Whitehead et al., 1988). Roberts (1984) described A. scintilla,the juvenile specimens were not utilised to limit ontogenetic effects, smallest clupeiform, as a paedomorphic species based on the loss or shape distortion and other non-biological variation. Fourteen homolo- reduction of various characters, particularly the reduction of the pelvic gous, two-dimensional landmarks were used to summarise body shape girdle. Although the phylogenetic placement of A. scintilla was uncertain using the program TPSdig 2.31 (Rohlf, 2009). The landmarks (Figure 2) at the time of description, Lavoué et al. (2010) demonstrated that included: (1) anterior end of the rostral organ (snout); (2) dorsal A. scintilla was a member of New World anchovies and Bloom and orbit; (3) ventral orbit; (4) posterior of supraoccipital bone of the Lovejoy (2012) determined this species is a member of a clade of fresh- neurocranium; (5) dorsal tip of the operculum; (6) ventral tip of water anchovies from South America. Cervigón (1982) described the sub-operculum; (7) anterior insertion of the pectoral fins; (8) A. manamensis and hypothesised a phylogenetic affinity with other anterior insertion of pelvic fins; (9) anterior insertion of anal fin; freshwater and estuarine members of Anchoviella from north-eastern (10) posterior insertion of anal fin; (11) posterior insertion of dorsal South America. Several studies have clarified the phylogenetic relation- fin; (12) anterior insertion of dorsal fin; (13) dorsal insertion of caudal ships of New World anchovies and inferred the phylogenetic positions fin; (14) ventral insertion of caudal peduncle. We tested for a signifi- of both A. scintilla and A. manamensis (Bloom & Lovejoy, 2012, 2014; cant effect of size on shape using Procrustes regression with permuta- Lavoué et al., 2010, 2013). tion (nperm = 1000) (procD.allometry function in geomorph 3.0.5; In this study we investigated the patterns and processes of pheno- Adams et al., 2018). This method estimates the effect, or covariation, typic evolution associated with miniaturisation. We reconstructed of centroid size with our Procrustes-aligned shape coordinates, using body-size evolution across New World anchovies to determine a linear model (Collyer et al., 2015). whether miniaturisation evolves
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